Original article

Effects of Aloe vera coating on postharvest quality of tomato Mario A. GARCÍA1*, Marisabel VENTOSA1, Raúl DÍAZ1, Silvia FALCO2, Alicia CASARIEGO1

1

Pharm. Food Inst., Univ. Havana, St. 222 No. 2317, Havana, Cuba, ZC 13600, [email protected] 2

Food Ind. Res. Inst., Carretera al Guatao km 3½, Havana, Cuba, ZC 19200

Effects of Aloe vera coating on postharvest quality of tomato. Abstract – Introduction. Edible coatings are traditionally used to improve food appearance and preservation. They act as barriers during processing, handling and storage, and do not solely retard food deterioration, enhancing its quality, but are safe due to natural biocide activity, or to the incorporation of antimicrobial compounds. The aim of this work was to evaluate the effect of A. vera, applied as an edible coating, on the changes in physicochemical parameters related to tomato fruit quality during storage in ambient conditions (22 °C and 80% RH), as well as its role in controlling microbial spoilage. Materials and methods. The changes in physical, chemical and textural properties of commercial tomato cv. Charleston were evaluated during a storage period of 17 days in ambient conditions according to their coating (treatments), or not (control), with an aqueous extract of pure A. vera or diluted (2:1) in distilled water. Results. The pure aqueous extract of Aloe vera totally inhibited the growth of Rhizoctonia solani and Alternaria alternata, while it did not show antimicrobial activity against Phytophthora parasitica. The diluted aqueous extract of Aloe vera coating maintained the quality of the tomatoes during storage in ambient conditions, delaying ripening, although it did not constitute an effective barrier against weight loss. Conclusion. Our fundamental results may be useful to breeders and postharvest technologists, as well as distributors, importers and exporters, in handling and processing tomatoes.

Cuba / Lycopersicon sculentum / fruits / keeping quality / edible films / Aloe vera / antimicrobial properties

Effets de l’enrobage d’Aloe vera sur la qualité post-récolte de la tomate. Résumé – Introduction. Des enrobages comestibles sont traditionnellement utilisés pour améliorer l’aspect et la conservation des aliments. Ils protègent les fruits au cours de leur transformation, leur manutention et leur stockage ; non seulement ils retardent la détérioration des aliments en améliorant leur qualité, mais ils sont également sans danger en raison de leur activité biocide naturelle ou de leur teneur en composés antimicrobiens. Le but de notre travail a été d’évaluer l’effet d’A. vera, appliqué comme revêtement comestible, sur l’évolution des paramètres physico-chimiques liés à la qualité de tomates pendant leur stockage en conditions ambiantes (22 °C et 80 % HR), ainsi que de déterminer son rôle dans le contrôle de la contamination microbienne. Matériel et méthodes. L’évolution des propriétés physiques, chimiques et texturales de tomates cv. Charleston du commerce a été évaluée au * Correspondence and reprints cours d’une période de stockage de 17 jours en conditions ambiantes en fonction de leur enrobage (traitements), ou non (témoin), avec un extrait aqueux d’A. vera pur ou dilué (2:1) dans de l’eau distillée. Résultats. L’extrait aqueux d’A. vera pur a inhibé totalement la croisReceived 21 January 2013 sance de Rhizoctonia solani et Alternaria alternata, mais il n’a pas montré d’activité antimiAccepted 4 July 2013 crobienne contre Phytophtora parasitica. Le revêtement avec l’extrait aqueux d’A. vera dilué a maintenu la qualité des tomates durant leur stockage en conditions ambiantes et il a retardé Fruits, 2014, vol. 69, p. 117–126 leur maturation, mais il n’a pas constitué une barrière efficace contre la perte de poids. Conclusion. Nos résultats pourraient s’avérer utile aux producteurs et techniciens de post© 2014 Cirad/EDP Sciences récolte, ainsi qu’aux distributeurs, importateurs et exportateurs, lors de la manutention et de All rights reserved la transformation de la tomate. DOI: 10.1051/fruits/2014001 www.fruits-journal.org RESUMEN ESPAÑOL, p. 126

Cuba / Lycopersicon sculentum / fruits / aptitude à la conservation / film comestible / Aloe vera / propriété antimicrobienne

Article published by EDP Sciences Fruits, vol. 69 (2)

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1. Introduction Tomato has become the model species for climateric fruit ripening, due to its commercial importance, easy genetic manipulation, rapid cycle and year-round non-seasonal greenhouse fruit production. Consequently, much of our understanding about the regulation of climateric fruit ripening comes from studies on tomato, although research in other species is also reported. Tomato quality changes continuously after harvesting. Fresh tomato quality is determined by appearance, color, firmness and flavor. The main quality indices are skin color, which is related to fruit ripening and affected by the lycopene concentration [1], and the total soluble solids-total acidity ratio attained at harvest. Fruit firmness is also an important quality attribute and is directly related to enhancement of storability potential and induction of greater resistance to decay and mechanical damage. Tomato fruits deteriorate rapidly after harvest and in some cases after transport and marketing, and thus do not reach consumers at optimum quality. The main causes of tomato deterioration are weight loss, color changes, softening, surface pitting and loss of acidity, while small variations occur in total soluble solids [2]. Finally, special care is needed with the occurrence of decay, which is mainly due to species of the genera Alternaria, Rhizopus, Botrytis, Geotrichum and Fusarium [3], which can cause great economic losses although the occurrence of rots and their influence on tomato quality have been reported to be dependent on the cultivar and ripening stage at harvest [4]. Several pre- and postharvest technologies have been used to control decay, but the postharvest use of chemicals as fungicides is restricted in most countries and consumers demand agricultural commodities without pesticide residues [5]. Among these technologies, edible coatings are traditionally used to improve food appearance and preservation [6]. They act as barriers during processing, handling and storage, and do not solely retard food deterioration and enhance its quality, but are also safe due to natural biocide activity, or

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to the incorporation of antimicrobial compounds [7]. Different compounds have mainly been used as edible coatings to prevent commodity weight loss, including wax, milk proteins, celluloses, lipids, starch, zein, alginate and chitosan [7, 8]. Edible coatings based on chitosan reduced weight loss and softening, and extended the shelf life of tomato [4, 9]. Currently, there is increasing interest in the use of Aloe vera gel in the food industry, being used as a source of functional foods in drinks, beverages and ice creams [10]. Nevertheless, the processing techniques used to obtain A. vera gel are very important to ensure the product quality and to maintain almost all the bioactive components [11]. Aloe vera gel is the mucilaginous gel obtained from the squeezing of the clear jelly-like substance of the parenchyma tissue of A. vera leaves. Aloe vera gel has been reported to have multiple beneficial properties for wound healing, including the abilities to penetrate and anesthetize tissue, and preclude bacterial, fungal and viral growth, and also acts as an antiinflammatory agent and enhances blood flow [12–16]. Aloe vera is well known for its polysaccharides and anthraquinone derivatives. Besides, two new dihydrocoumarin derivatives with strong antioxidant activity were isolated [17]. This activity could also be shown for some aloesin derivatives, e.g., isorabaichromone, feruloylaloesin and pcoumaroylaloesin [18]. It was reported [19] that the use of A. vera gel coating preserves the functional properties of table grapes, according to their developed patent [20]. In addition, the use of an edible coating based on A. vera gel as a postharvest treatment to maintain sweet cherry [21] and nectarine [22] quality and safety was reported. Aloe vera gel, used as an edible coating in fruit, would be an innovative and interesting means for commercial application and an alternative to the use of postharvest chemical treatments. The aim of our work was to evaluate the effect of A. vera, applied as an edible coating, on the changes in physicochemical parameters related to tomato

Aloe vera coating of tomato

fruit quality during storage in ambient conditions, as well as its role in controlling microbial spoilage.

incubation at 30 °C. The experiment was carried out in triplicate.

2.2. Plant material and experimental design

2. Materials and methods 2.1. Qualitative evaluation of antimicrobial activity of the aqueous extract of A. vera 2.1.1. Microorganisms tested Pathogenic microorganisms were selected for the study on the basis of their potential to cause contamination of fruit and vegetables. The fungal strains used for the screening were Rhizoctonia solani spp., Alternaria alternata spp. and Phytophthora parasitica spp. 2.1.2. Determination of antimicrobial activity Culture tubes with 5 mL of sterile peptone water (0.01%, w/v) were inoculated with strains of fungi. The suspension was stirred vigorously using a magnetic stirrer and placed in contact with the aqueous extract of A. vera (pharmaceutical quality, 100% purity) manufactured by Pharmaceutical Laboratories Mario Muñoz (Havana, Cuba) with the following characteristics: – liquid from yellow to dun-reddish colors with a characteristic odor, – pH 4.8, – soluble solids: 0.732%, – total polysaccharides: 0.288%, – density: 1.004 g⋅mL–1, – bacteria (Bacillus Gram +) counts: inferior to 10 UFC⋅mL–1, – fungi counts: 23 UFC⋅mL–1. The dilution agar method was used for this study. Each plate, containing Potato Dextrose Agar (PDA), was seeded with 1 mL of spore suspension of fungi. The antimicrobial activity was evaluated by observing the total or partial inhibition in the growth of the microorganism after 5 days of

Tomato fruits (Lycopersicon sculentum cv. Charleston) were harvested from a commercial farm and characterized. At the laboratory, fruits were selected, based on homogeneous colour (breaker stage) according to color standards for tomato [23], and size, absence of injuries and fungal infection. Some of them were used to analyze properties at harvest and the remainder were randomly divided into three batches. One of them was treated with A. vera L. aqueous extract (100% purity) and the second batch was treated with a solution of A. vera L. aqueous extract diluted 2:1 with distilled water. The treatment was performed at 22 °C by double immersion for 2 min in film-forming solutions. The other batch was immersed in distilled water and served as the control. Following the treatment, tomatoes were air-dried, packaged in perforated corrugated cardboard boxes and stored in ambient conditions (22 °C and 80% RH). Samples of each treatment, coated and uncoated, were taken out after (3, 5, 7, 10, 12, 14 and 17) days of storage and were immediately analyzed for quality and storage potential.

2.3. Quality attributes 2.3.1. Classification according to ripening stages The tomatoes were classified according to their ripening stage using a visual scale [24]. The results were expressed as percentage of tomatoes in each ripening stage established by treatment. 2.3.2. pH, titrable acidity and soluble solids content After firmness analysis, tomatoes were cut into small pieces and homogenized in a grinder, and 10 g of ground tomato were suspended in 100 mL of distilled water and then filtered. The pH and titratable acidity

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Table I. Qualitative evaluation of antimicrobial activity of the aqueous extract of Aloe vera. Microorganisms

Distilled water

Aqueous extract of Aloe vera

Rhizoctonia solani

Without antimicrobial activity

Antimicrobial activity

Alternaria alternata

Without antimicrobial activity

Antimicrobial activity

Phytophthora parasitica

Without antimicrobial activity

Without antimicrobial activity

of the samples were assessed using a pH meter (Basic 20, Crison) [25] and titrated using 0.1 N NaOH. Titratable acidity was expressed as g citric acid⋅100 g–1 of tomato weight [26]. The soluble solids content was determined in the juice of ground tomatoes by an Atago RX-1000 digital refractometer (Atago Co. Ltd., Tokyo, Japan) at 25 °C and expressed as °Brix [27]. Measurements were made in triplicate. 2.3.3. Texture analysis The instrument used was a cone penetrometer with a 30° cone angle (A. H. Thomas Co., USA). The mass of the cone assembly was 150 g. The penetration time used was 5 s [28]. Four replicates in an individual sample were done for each treatment. Each fruit was measured in the central zone. Firmness was measured as the maximum penetration distance reached during penetration time.

up to 10% of dehydrated surface; D2, up to 30% of dehydrated surface; D3, more than 30% of dehydrated surface; and D4, excess ripening with visible fungal decay. Tomato fruits showing surface mycelial development were considered decayed. The tomato fruits that showed D3 or D4 dehydration levels were considered as deteriorated units. The results were expressed as percentage of damaged products.

2.4. Statistical analysis All the experiments were performed in triplicate. Two-way ANOVA was performed using STATISTICS software [30] and Duncan’s multiple range test was used for comparing differences among mean values. Mean values were reported, and the significance was defined at p ≤ 0.05.

2.3.4. Weight loss and moisture content Tomatoes were weighed at the beginning of the experiment just after coating and air-drying, and thereafter each sampling day during the storage period. Weight loss was expressed as the percentage loss of the initial total weight. For each measurement, 15 fruits corresponding to each treatment were used. Moisture content was determined gravimetrically by drying 2.5 g of tomato samples in an oven at 105 °C until a constant weight was measured [29]. 2.3.5. Physiological and fungal decay The physiological decay of tomatoes was inspected visually at the end of the storage, evaluating the skin dehydration level (D1, D2, D3 and D4) of the products, D1 being

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3. Results and discussions 3.1. Antimicrobial activity of the aqueous extract of Aloe vera The evaluation of the antimicrobial activity of the aqueous extract of A. vera against Rhizoctonia solani, Alternaria alternata and Phytophthora parasitica showed that the aqueous extract of A. vera totally inhibited the growth of R. solani and A. alternata, while it did not have any effect against P. parasitica (table I). The antifungal activity of A. vera has been reported against postharvest fruit pathogens, such as Penicillium digitatum, P. expansum, B. cinerea and A. alternata [31] and was based on the suppression of

Aloe vera coating of tomato

germination and the inhibition of mycelial growth [21]. In addition, the inhibitory effects of several Aloe extracts have also been found on Aspergillus niger, Cladosporium herbarum and Fusarium moniliforme, and could be attributed mainly to the presence of Aloe-emodin and aloenin together with other active compounds [32], although the specific mechanism of action is still unknown. Moreover, the reduction of the growth of 17 bacteria by A. vera gel has been proven [15], being more effective against Gram-positive than Gram-negative microorganisms [33]. Some individual components found in A. vera gel, such as saponins, acemannan and anthraquinone derivatives, are known to have antibiotic activity, and could be responsible for its antibacterial activity.

Figure 1. Changes in ripening degree of tomatoes as a function of storage time at 22 °C for uncoated fruits (control) and fruits coated with A. vera L. aqueous extract, either pure, or diluted 2:1 with distilled water.

3.2. Classification according to ripening stages Figure 2. Changes in pH of tomatoes as a function of storage time at 22 °C for uncoated fruits (control) and fruits coated with A. vera L. aqueous extract, either pure, or diluted 2:1 with distilled water. Vertical bars indicate confidence intervals (n = 3).

If we keep in consideration that the tomato variety studied (L. sculentum cv. Charleston) does not have a long life and that its commercialization cycle is between (10 and 12) days in refrigeration at 6–8 °C, it was found that the treatment of tomatoes coated with the non-diluted A. vera L. aqueous extract (T1) was the most effective; indeed, in this treatment, tomatoes in ripening state 4 were observed until the 12th day of storage, while in the control fruits (TC) and in the tomatoes coated with A. vera L. aqueous extract diluted 2:1 (T2), higher percentages of tomatoes in more advanced ripening states (5 and 6) existed (figure 1).

Figure 3. Changes in acidity content of tomatoes as a function of storage time at 22 °C for uncoated fruits (control) and fruits coated with A. vera L. aqueous extract, either pure, or diluted 2:1 with distilled water. Vertical bars indicate confidence intervals (n = 3).

3.3. pH, titratable acidity and soluble solids content The pH values showed a significant increase (p ≤ 0.05) during the first two weeks of the experiment; a decrease in these values toward the end of the storage period took place, while no significant differences (p ≤ 0.05) were observed among treatments (figure 2). pH values between 4 and 4.4 for tomatoes cv. FA-180 coated with chitosan were reported [34]; similar results were

found in the present study, where the values oscillated between 4.2 and 4.6. No significant differences (p ≤ 0.05) were observed between coated samples for changes in titratable acidity values (figure 3), but these samples differed significantly (p ≤ 0.05) with the values obtained for

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Table II. Changes in soluble solids content (°Brix) of tomatoes as a function of storage time at 22 °C (n = 3). Mean (standard deviation). Time (d)

Control

Treatments with Aloe vera L. aqueous extract Without dilution

Diluted 2:1 with distilled water

0

2.57 (0.10) a

2.57 (0.10) a

2.57 (0.10) a

10

3.17 (0.10) c

2.87 (0.05) b

3.17 (0.05) c

14

3.67 (0.05) d

2.57 (0.05) a

3.83 (0.05) d

17

3.83 (0.10) d

3.27 (0.05) c

3.63 (0.20) d

Different letters in the same column differ significantly (p ≤ 0.05).

Figure 4. Effect of Aloe vera coatings on the firmness of tomatoes stored at 22 °C for uncoated fruits (control) and fruits coated with A. vera L. aqueous extract, either pure, or diluted 2:1 with distilled water. Vertical bars indicate confidence intervals (n = 4).

uncoated samples. As can be observed, there was a correspondence between the behavior of the titratable acidity and pH values, respectively, during the storage. The uncoated tomatoes, although they were the most ripe, presented higher titratable acidity values than coated tomatoes, which coincides with reports by other authors [34]. The small differences found in pH and titratable acidity values during storage between uncoated and coated tomatoes could be related to the loss of water by samples since titratable acidity is given as a percentage of citric acid per tomato wet weight. The soluble solids content is the index that most affects the yield during the elaboration of tomato products. Nevertheless, it is reported that this indicator increases, but not considerably, during the ripening of tomato fruits [35]. Changes in the soluble solids content of tomatoes over the storage period showed an increase (p ≤ 0.05) during the storage, being significantly higher (p ≤ 0.05) in uncoated tomatoes and those coated with diluted extract of A. vera

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(table II). This observation could be associated with the differences observed in the ripening state (figure 1). The increase in the soluble solids content of tomatoes is related to changes in the cellular wall, especially the pectic substances and hemicellulose [36], associated with changes in the firmness of tomato fruits. Samples coated with the pure extract of A. vera showed a lower increase in soluble solids content. An increase in soluble solids content in control and coated tomatoes was also reported [37]. It can be expected that soluble solids content increases during tomato ripening and decreases in mature fruit due to respiration [38]. The [soluble solids content / titratable acidity] ratio is considered as a ripening index for citric fruits; however, in tomato, this index is used as an indicator of flavor [1]. In this case, this ratio was mostly influenced by the soluble solids content values, since the titratable acidity had almost no change among treatments during storage. These results coincide with those reported by other authors [34, 39].

3.4. Firmness When studying the changes in the firmness, evaluated as penetration distance, of control and treated fruits during the storage period of 17 days at 22 °C, all the samples presented similar initial firmness values (p ≤ 0.05) and lost their firmness gradually during the storage period (p ≤ 0.05) (figure 4). The loss of firmness during the storage period is a normal behavior during the maturation of tomatoes, since it has been

Aloe vera coating of tomato

Table III. Loss of weight (%) of tomatoes as a function of storage time at 22 °C. Mean (standard deviation). Time (d)

Control

3

Treatments with Aloe vera L. aqueous extract Without dilution

Diluted 2:1 with distilled water

0.8 (0.2)

0.8 (0.2)

0.7 (0.2)

5

1.6 (0.4)

1.7 (0.5)

1.4 (0.5)

7

2.4 (0.6)

2.5 (0.8)

2.3 (0.7)

10

3.4 (0.9)

3.6 (1.0)

3.2 (1.0)

12

4.1 (1.0)

4.3 (1.0)

3.9 (1.0)

14

4.6 (1.0)

4.9 (1.0)

4.5 (1.0)

17

5.6 (1.0)

5.8 (1.0)

5.4 (1.0)

reported that the increase in the ethylene concentration in this stage promotes the synthesis of polygalacturonase, the enzyme responsible for softening [40]. Aloe vera coatings exerted a beneficial effect on fruit firmness such that, by the end of the storage period, both the treatments gave rise to fruit with higher firmness values than untreated fruit (p ≤ 0.05) (figure 4). Some authors reported similar results for table grapes and cherries coated with A. vera gel diluted 1:3, observing a delay in the loss of firmness as well as in the evolution of the color and an increment in the ripening index ([SSC/TA] ratio) in the coated fruits, mostly due to the fact that the coatings lowered the respiration rate during postharvest storage [21, 41].

3.5. Weight loss and moisture content All treatments showed a gradual loss of weight during storage (table III). As can be observed, the coating of A. vera aqueous extract did not delay (p ≤ 0.05) the moisture loss, this effect being similar to those obtained with other edible coatings [34]. Although the A. vera coatings did not reduce the weight loss, the values of this parameter did not affect, in any of the cases, the quality of stored fruits, considering as an index of the end of the shelf life in tomato a physiological loss of weight of 10% [42, 43].

Figure 5. Changes in humidity content of tomatoes as a function of storage time at 22 °C for uncoated fruits (control) and fruits coated with A. vera L. aqueous extract, either pure, or diluted 2:1 with distilled water. Vertical bars indicate confidence intervals (n = 3).

The moisture content showed a significant reduction (p ≤ 0.05) for all treatments during the storage (figure 5), while significant differences (p ≤ 0.05) between coated and uncoated samples were not observed. In contrast with our results for weight loss during storage, it was reported that the A. vera gel coating was effective as a physical barrier and thus reduced the weight loss and lowered the respiration rate during the postharvest storage of table grapes and cherries, respectively [21, 41]. The mechanism for these positive effects is based on their hygroscopic properties, which enables formation of a barrier to water diffusion between the fruit and the environment, thus avoiding its external transference [44]. Composite coatings of polysaccharide-lipid are known to increase water barrier efficacy with increased lipid content and in turn more reduction of weight loss could be achieved [45]. However, A. vera gel, the

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Table IV. Loss of fruit (%) due to physiological and fungal decay at the end of the storage at 22 °C during 17 days. Treatments

Dehydrated surface Total Until 10%

Until 30%

> 30%

18.75

25

43.75

87.50

Without dilution

31.25

25

18.75

75

Diluted 2:1 with distilled water

43.75

25

6.25

75

Control Treatments with Aloe vera L. aqueous extract

composition of which is mainly polysaccharides [46], was highly effective as a moisture barrier without the lipid incorporation.

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3.6. Loss of fruit due to physiological and fungal decay Aspect is a critical quality attribute in the consumer acceptability of fresh fruit and vegetables. When considering the losses of fruit due to physiological and fungal decay at the end of the storage, we observed that uncoated and coated tomatoes did not show signs of fungal decay after the storage at 22 °C for 17 days (table IV); nevertheless, the control units (TC) showed the biggest percentages of wrinkled tomatoes by dehydration, although there were no significant differences (p ≤ 0.05) in the weight loss among treatments (table IV); additionally, the uncoated tomatoes presented the lowest firmness values (figure 4).

4. Conclusion The pure aqueous extract of Aloe vera totally inhibited the growth of Rhizoctonia solani and Alternaria alternata, while it did not show antimicrobial activity against Phytophthora parasitica. The aqueous extract of Aloe vera coating, with respect to the diluted extract, maintained the stability of the tomatoes cv. Charleston during storage in ambient conditions, delaying the ripening, although it did not constitute an effective barrier against weight loss.

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Efectos del recubrimiento con Aloe vera en la calidad poscosecha de tomate. Resumen – Introducción. Los recubrimientos comestibles son usados tradicionalmente para mejorar la apariencia y conservación de los alimentos. Actúan como barreras durante el procesamiento, manipulación y almacenamiento y no solo retardan su deterioro incrementando su calidad, sino también su seguridad a través de su actividad biocida natural o por la incorporación de compuestos antimicrobianos. El objetivo de este trabajo fue evaluar el efecto del A. vera, aplicado como recubrimiento comestible sobre los cambios en los parámetros físicoquímicos relacionados con la calidad de tomates durante su almacenamiento en condiciones ambientales (22 °C y 80 % HR), así como su papel en el control del deterioro microbiológico. Material y métodos. Se evaluaron los cambios en las propiedades físicas, químicas y texturales de tomates comerciales var. Charleston durante 17 días de almacenamiento en condiciones ambientales de acuerdo a sus recubrimientos (tratamientos) o no (control), con extracto acuoso de A. vera puro o diluido (2:1) en agua destilada. Resultados. El extracto acuoso puro de A. vera inhibió, totalmente, el crecimiento de Rhizoctonia solani and Alternaria alternata, mientras que no mostró actividad antimicrobiana contra Phytophtora parasitica. El recubrimiento de extracto acuoso diluido de A. vera mantuvo al calidad de los tomates durante su almacenamiento en condiciones ambientales, retardando su maduración, aunque no constituyó una barrera efectiva contra las pérdidas de peso. Conclusión. Nuestros resultados fundamentales pueden ser útiles para productores y tecnólogos poscosecha, así como distribuidores, importadores y exportadores, relacionados con el manejo y procesamiento de tomates.

Cuba / Lycopersicon sculentum / frutas / aptitud para la conservación / film comestible / Aloe vera / propiedades antimicrobianas

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